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Chloroplast Biogenesis During Rehydration of the Resurrection Plant Xerophyta Humilis: Parallels to the Etioplast–Chloroplast Transition

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Chloroplast Biogenesis During Rehydration of the Resurrection Plant Xerophyta Humilis: Parallels to the Etioplast–Chloroplast Transition Plant, Cell and Environment (2008) 31, 1813–1824 doi: 10.1111/j.1365-3040.2008.01887.x Chloroplast biogenesis during rehydration of the resurrection plant Xerophyta humilis: parallels to the etioplast–chloroplast transition ROBERT A. INGLE1*, HELEN COLLETT1*, KEREN COOPER1, YUICHIRO TAKAHASHI2, JILL M. FARRANT1 & NICOLA ILLING1 1Department of Molecular and Cell Biology, University of Cape Town, Private Bag, Rondebosch 7701, South Africa and 2The Graduate School of Natural Science and Technology, Okayama University, 3-1-1 Tsushima-naka, Okayama 700-8530, Japan •- ABSTRACT initially the superoxide radical (O2 ) and singlet oxygen 1 ( O2) (Ivanov & Khorobrykh 2003; Møller, Jensen & De-etiolation of dark-grown seedlings is a commonly used Hansson 2007), and chloroplasts contain several antioxi- experimental system to study the mechanisms of chloro- dant systems to scavenge ROS (Apel & Hirt 2004; Foyer & plast biogenesis, including the stacking of thylakoid mem- Noctor 2005). The equilibrium between ROS production branes into grana, the response of the nuclear-chloroplast and scavenging can be perturbed by environmental stresses transcriptome to light, and the ordered synthesis and leading to a rapid increase in ROS concentration (Apel & assembly of photosystem II (PSII). Here, we present the Hirt 2004; Møller et al. 2007). Under water-deficit stress, xeroplast to chloroplast transition during rehydration of the especially under high-light conditions, the excitation energy Xerophyta humilis resurrection plant as a novel system for harvested by chlorophyll can greatly exceed the demand of studying chloroplast biogenesis, and investigate the role of the Calvin cycle for ATP and NADPH, leading to overre- light in this process. Xeroplasts are characterized by the duction of the electron transport chain and enhanced gen- presence of numerous large and small membrane-bound eration of ROS (Smirnoff 1993; Apel & Hirt 2004; Møller vesicles and the complete absence of thylakoid membranes. et al. 2007). While ROS play critical roles in cell signalling While the initial assembly of stromal thylakoid membranes (Kovtun et al. 2000; Foyer & Noctor 2005), they can also occurs independently of light, the formation of grana is light cause extensive oxidative damage to macromolecules such dependent. Recovery of photosynthetic activity is rapid in as lipids, proteins and nucleic acids (Møller et al. 2007). plants rehydrated in the light and correlates with the light- Resurrection plants, which are able to tolerate the loss of dependent synthesis of the D1 protein, but does not require 95% of protoplasmic water and recover full metabolic de novo chlorophyll biosynthesis. Light-dependent synthe- activity in existing tissues upon rehydration, avoid a toxic sis of the chlorophyll-binding protein Lhcb2 and digalacto- build-up of ROS by a controlled and reversible shutdown of syldiacylglycerol synthase 1 correlated with the formation photosynthesis early on during the drying process (Sherwin of grana and with the increased PSII activity. Our results & Farrant 1998; Farrant 2000). suggest that the molecular mechanisms underlying photo- Angiosperm resurrection plants can be classified into two morphogenic development may also function in desiccation groups based on the mechanisms they utilize to shut down tolerance in poikilochlorophyllous resurrection plants. photosynthesis during desiccation. Homoiochlorophyllous species, such as Craterostigma, retain their chlorophyll and Key-words: desiccation tolerance; photosynthesis; resurrec- rely on pigment production and morphological changes, tion plant; xeroplast. such as leaf folding, to prevent light–chlorophyll interac- tions during desiccation (Sherwin & Farrant 1998; Farrant 2000). In contrast, poikilochlorophyllous resurrection INTRODUCTION plants, such as Xerophyta, dismantle thylakoid membranes The light reactions of photosynthesis couple the absorption and break down chlorophyll during drying (Tuba et al. 1996; of light by chlorophyll to the generation of energy and Sherwin & Farrant 1998; Farrant 2000). Recent studies have indicated that down-regulation of reducing power to drive the fixation of CO2 (Nelson & Yocum 2006). Operation of the light reactions inevitably photosystem II (PSII) subunit expression also occurs in leads to the formation of reactive oxygen species (ROS), poikilochlorophyllous species during desiccation (Collett et al. 2004; Ingle et al. 2007). PSII is a large protein complex Correspondence: N. Illing. Fax: +27 21 689 7573; e-mail: located predominately in the granal thylakoid membranes [email protected] of the chloroplast, and contains approximately 25 protein *These authors contributed equally to this work. subunits encoded by the psb genes (Mullineaux 2005; © 2008 The Authors Journal compilation © 2008 Blackwell Publishing Ltd 1813 1814 R. A. Ingle et al. Nelson & Yocum 2006). Six psb genes were previously Determination of RWC identified as desiccation down-regulated in a small-scale Absolute water content (AWC) of leaf samples was calcu- microarray analysis of Xerophyta humilis gene expression. lated using the formula (fresh biomass–dry biomass)/dry These included psbA, which encodes the D1 subunit of the biomass. RWC was calculated using the formula (AWC PSII core complex, and psbO and psbP, which encode com- ¥ 100)/AWC at full turgor (determined after bagging the ponents of the oxygen-evolving complex (OEC). A reduc- control plants overnight after watering). Ten leaf samples tion in protein levels of several PSII subunits in Xerophyta were taken at each time point from each treatment group viscosa at 55% relative water content (RWC) correlated for determination of RWC. with the cessation of photosynthetic activity in this species (Ingle et al. 2007). Upon rehydration, photochemical activity recovers Determination of chlorophyll content rapidly in Xerophyta species (Sherwin & Farrant 1996), The leaf samples were cut into small pieces, and chlorophyll suggesting that they have evolved mechanisms to allow the was extracted in 100% acetone for 4 d at 4 °C. Total rapid biogenesis and assembly of both thylakoid mem- chlorophyll (a + b) content (mg g DW-1) was determined branes and the photosynthetic apparatus. The molecular spectrophotometrically using the equation (7.05 ¥ A661.6) + basis of this process and the signalling events involved (18.09 ¥ A644.8) as described in Lichtenthaler (1987). are unclear, although the role of water availability is ob- vious. Strikingly, similar processes occur in the etioplast– chloroplast transition during photomorphogenesis when Measurement of PSII operating efficiency light acts as the signal for chlorophyll biosynthesis, forma- The quantum yield of photosystem II (FPSII), the propor- tion and stacking of thylakoid membranes, and translation tion of light absorbed by the PSII antennae used in photo- of several PSII mRNAs including psbA, psbB and psbC chemistry (Genty, Briantais & Baker 1989), was determined (Klein & Mullet 1987; von Wettstein, Gough & Kannangara by measurement of chlorophyll fluorescence using a PAM- 1995; Baena-Gonzalez & Aro 2002). Here, we present the 2100 portable chlorophyll fluorometer (Heinz-Walz GmbH, reassembly of chloroplasts during rehydration of X. humilis Effeltrich, Germany). The leaf samples were light adapted as a novel system to study chloroplast biogenesis, and dem- at a photosynthetic flux of ~50 mmol m-2 s-1 for 15 min prior onstrate the role of light in several key events in this to measurement of FPSII. process. CO2 measurements MATERIALS AND METHODS The rate of net CO2 assimilation or release was determined Plant material and culture using an LI-6400 portable photosynthesis system (Li-Cor Biosciences, Lincoln, NE, USA), operated at an ambient Xerophyta humilis plants were collected from Borakalalo CO2 concentration of 350 ppm. The parameters A and National Park (Limpopo Province, South Africa), potted Rd were calculated using the equations described by von and grown under glasshouse conditions as described in Caemmerer & Farquhar (1981). Sherwin & Farrant (1996). Prior to this study, the plants were transferred to a controlled environment room with a photosynthetic flux of ~200 mmol m-2 s-1 under a 16 h Chloroplast ultrastructural studies light/8 h dark cycle at 25 °C. The plants were dried down Chloroplast ultrastucture was examined using transmission by withholding water for 2 weeks, and then kept in a electron microscopy as previously described in Cooper & desiccated state for a further 2 weeks prior to rehydra- Farrant (2002). Briefly, small pieces of leaf tissue (approxi- tion. Hydrated (control) plants were regularly watered mately 2 mm2) were excised from the middle of four differ- throughout. Light-excluding boxes were placed over the ent leaves, and RWC was determined for each leaf. Fixation plants the previous evening for the rehydration in the was carried out in 2.5% glutaraldehyde in 0.1 m phosphate dark experiments. buffer (pH 7.4) containing 0.5% caffeine, and samples were postfixed in 1% osmium in phosphate buffer.After dehydra- Rehydration time course tion in a graded ethanol series, the tissue was infiltrated with epoxy resin over 4 d. The samples were embedded in epoxy Desiccated plants were rehydrated under a normal 16 h resin, hardened at 60 °C for 16 h, and sectioned at a gold light/8 h dark cycle or in continuous darkness, beginning 1 h interference colour (95 nm) using a microtome. Sections prior to ‘dawn’. Each rehydration experiment spanned a were stained with 2% uranyl aceate and
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